Taste Preferences at Different Ambient Temperatures and Associated Changes in Gut Microbiota and Body Weight in Mice
Abstract
1. Introduction
2. Materials and Methods
2.1. Animal Design
2.2. Gut Microbiota Analysis
2.3. Beta Diversity Analysis
2.4. Predicted Metagenome
2.5. Statistical Analysis
3. Results
3.1. Taste Preference and Weight Changes
3.2. Changes in Gut Microbiota Structure Associated with Food Flavors
3.3. The Correlations of Ambient Temperature, Tastes, and Bacterial Taxa
3.4. Functional Diversity among the Different Taste Treatments under Different Temperature Conditions
4. Discussion
4.1. Dietary Preferences and Weight Change
4.2. Impact of Different Tastes on the Function of Gut Microbiota
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Negri, R.; Di Feola, M.; Di Domenico, S.; Scala, M.G.; Artesi, G.; Valente, S.; Smarrazzo, A.; Turco, F.; Morini, G.; Greco, L. Taste perception and food choices. J. Pediatr. Gastroenterol. Nutr. 2012, 54, 624–629. [Google Scholar] [CrossRef] [PubMed]
- Sousa Lima, R.; Cazelatto de Medeiros, A.; Andre Bolini, H.M. Does the indoor thermal environment influence the dominant sensation in a functional beverage attribute? J. Food Sci. 2020, 85, 3536–3542. [Google Scholar] [CrossRef] [PubMed]
- Jacques, A.; Chaaya, N.; Beecher, K.; Ali, S.A.; Belmer, A.; Bartlett, S. The impact of sugar consumption on stress driven, emotional and addictive behaviors. Neurosci. Biobehav. Rev. 2019, 103, 178–199. [Google Scholar] [CrossRef] [PubMed]
- Żebrowska, E.; Chabowski, A.; Zalewska, A.; Maciejczyk, M. High-Sugar Diet Disrupts Hypothalamic but Not Cerebral Cortex Redox Homeostasis. Nutrients 2020, 12, 3181. [Google Scholar] [CrossRef] [PubMed]
- Roura, E.; Foster, S.; Winklebach, A.; Navarro, M.; Thomas, W.; Campbell, K.; Stowasser, M. Taste and hypertension in humans: Targeting cardiovascular disease. Curr. Pharm. Des. 2016, 22, 2290–2305. [Google Scholar] [CrossRef]
- Beh, B.K.; Mohamad, N.E.; Yeap, S.K.; Ky, H.; Boo, S.Y.; Chua, J.Y.H.; Tan, S.W.; Ho, W.Y.; Sharifuddin, S.A.; Long, K. Anti-obesity and anti-inflammatory effects of synthetic acetic acid vinegar and Nipa vinegar on high-fat-diet-induced obese mice. Sci. Rep. 2017, 7, 6664. [Google Scholar] [CrossRef]
- Fan, Y.; Pedersen, O. Gut microbiota in human metabolic health and disease. Nat. Rev. Microbiol. 2021, 19, 55–71. [Google Scholar] [CrossRef]
- Turner, A.; Veysey, M.; Keely, S.; Scarlett, C.; Lucock, M.; Beckett, E.L. Interactions between Bitter Taste, Diet and Dysbiosis: Consequences for Appetite and Obesity. Nutrients 2018, 10, 1336. [Google Scholar] [CrossRef]
- Xie, F.; Shen, J.; Liu, T.; Zhou, M.; Johnston, L.J.; Zhao, J.; Zhang, H.; Ma, X. Sensation of dietary nutrients by gut taste receptors and its mechanisms. Crit. Rev. Food Sci. Nutr. 2023, 63, 5594–5607. [Google Scholar] [CrossRef]
- Wessels, A.G. Influence of the gut microbiome on feed intake of farm animals. Microorganisms 2022, 10, 1305. [Google Scholar] [CrossRef]
- Wang, Y.; Geng, R.; Zhao, Y.; Fang, J.; Li, M.; Kang, S.-G.; Huang, K.; Tong, T. The gut odorant receptor and taste receptor make sense of dietary components: A focus on gut hormone secretion. Crit. Rev. Food Sci. Nutr. 2023, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Arantes, R.; Alves, E.; Bicho, M.; Valente, A. The Possible Influence of Microbiota on Food Compulsion. J. Biomed. Sci. 2020, 2, 353–358. [Google Scholar]
- Lu, B.; Breza, J.M.; Contreras, R.J. Temperature influences chorda tympani nerve responses to sweet, salty, sour, umami, and bitter stimuli in mice. Chem. Senses 2016, 41, 727–736. [Google Scholar] [CrossRef] [PubMed]
- Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016, 4, e2584. [Google Scholar] [CrossRef]
- Parks, D.H.; Tyson, G.W.; Hugenholtz, P.; Beiko, R.G. STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics 2014, 30, 3123–3124. [Google Scholar] [CrossRef] [PubMed]
- den Hartigh, L.J.; Gao, Z.; Goodspeed, L.; Wang, S.; Das, A.K.; Burant, C.F.; Chait, A.; Blaser, M.J. Obese mice losing weight due to trans-10, cis-12 conjugated linoleic acid supplementation or food restriction harbor distinct gut microbiota. J. Nutr. 2018, 148, 562–572. [Google Scholar] [CrossRef] [PubMed]
- Sijtsema, S.J.; Reinders, M.J.; Hiller, S. Fruit and snack consumption related to sweet, sour and salty taste preferences. Br. Food J. 2012, 114, 1032–1046. [Google Scholar] [CrossRef]
- Jitrapakdee, S. Transcription factors and coactivators controlling nutrient and hormonal regulation of hepatic gluconeogenesis. Int. J. Biochem. Cell Biol. 2012, 44, 33–45. [Google Scholar] [CrossRef] [PubMed]
- Stein, L.J.; Cowart, B.J.; Beauchamp, G.K. The development of salty taste acceptance is related to dietary experience in human infants: A prospective study. Am. J. Clin. Nutr. 2012, 95, 123–129. [Google Scholar] [CrossRef] [PubMed]
- Mennella, J.A.; Finkbeiner, S.; Lipchock, S.V.; Hwang, L.-D.; Reed, D.R. Preferences for salty and sweet tastes are elevated and related to each other during childhood. PLoS ONE 2014, 9, e92201. [Google Scholar] [CrossRef]
- Gutierrez, R.; Fonseca, E.; Simon, S.A. The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity. Cell. Mol. Life Sci. 2020, 77, 3469–3502. [Google Scholar] [CrossRef]
- Ribeiro, G.; Oliveira-Maia, A.J. Sweet taste and obesity. Eur. J. Intern. Med. 2021, 92, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Mähler, A.; Klamer, S.; Maifeld, A.; Bartolomaeus, H.; Markó, L.; Chen, C.-Y.; Forslund, S.K.; Boschmann, M.; Müller, D.N.; Wilck, N. Increased salt intake decreases diet-induced thermogenesis in healthy volunteers: A randomized placebo-controlled study. Nutrients 2022, 14, 253. [Google Scholar] [CrossRef] [PubMed]
- Do, M.H.; Lee, H.-B.; Oh, M.-J.; Jhun, H.; Ha, S.K.; Park, H.-Y. Consumption of salt leads to ameliorate symptoms of metabolic disorder and change of gut microbiota. Eur. J. Nutr. 2020, 59, 3779–3790. [Google Scholar] [CrossRef]
- Cocores, J.A.; Gold, M.S. The Salted Food Addiction Hypothesis may explain overeating and the obesity epidemic. Med. Hypotheses 2009, 73, 892–899. [Google Scholar] [CrossRef]
- Fujiyama, R.; Toda, K. Functional effects of cold stimulation on taste perception in humans. Odontology 2017, 105, 275–282. [Google Scholar] [CrossRef] [PubMed]
- Forde, C.G. Flavor perception and satiation. In Flavor; Woodhead Publishing: Sawston, UK, 2016; pp. 251–276. [Google Scholar]
- Gupta, C.C.; Ferguson, S.A.; Aisbett, B.; Dominiak, M.; Chappel, S.E.; Sprajcer, M.; Fullagar, H.H.; Khalesi, S.; Guy, J.H.; Vincent, G.E. Hot, tired and hungry: The snacking behaviour and food cravings of firefighters during multi-day simulated wildfire suppression. Nutrients 2020, 12, 1160. [Google Scholar] [CrossRef]
- Quiniou, N.; Dubois, S.; Noblet, J. Voluntary feed intake and feeding behaviour of group-housed growing pigs are affected by ambient temperature and body weight. Livest. Prod. Sci. 2000, 63, 245–253. [Google Scholar] [CrossRef]
- Leung, R.; Covasa, M. Do Gut Microbes Taste? Nutrients 2021, 13, 2581. [Google Scholar] [CrossRef]
- Melaku, M.; Zhong, R.; Han, H.; Wan, F.; Yi, B.; Zhang, H. Butyric and Citric Acids and Their Salts in Poultry Nutrition: Effects on Gut Health and Intestinal Microbiota. Int. J. Mol. Sci. 2021, 22, 10392. [Google Scholar] [CrossRef]
- Fikry, A.M.; Attia, A.I.; Ismail, I.E.; Alagawany, M.; Reda, F.M. Dietary citric acid enhances growth performance, nutrient digestibility, intestinal microbiota, antioxidant status, and immunity of Japanese quails. Poult. Sci. 2021, 100, 101326. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Fattah, S.A.; El-Sanhoury, M.H.; El-Mednay, N.M.; Abdel-Azeem, F. Thyroid Activity, Some Blood Constituents, Organs Morphology and Performance of Broiler Chicks Fed Supplemental Organic Acids. Int. J. Poult. Sci. 2008, 7, 678–687. [Google Scholar] [CrossRef]
- Vacca, M.; Celano, G.; Calabrese, F.M.; Portincasa, P.; Gobbetti, M.; De Angelis, M. The Controversial Role of Human Gut Lachnospiraceae. Microorganisms 2020, 8, 573. [Google Scholar] [CrossRef]
- Serino, M.; Nicolas, S.; Trabelsi, M.S.; Burcelin, R.; Blasco-Baque, V. Young microbes for adult obesity. Pediatr. Obes. 2017, 12, e28–e32. [Google Scholar] [CrossRef] [PubMed]
- Meng, C.; Feng, S.; Hao, Z.; Dong, C.; Liu, H. Changes in gut microbiota composition with age and correlations with gut inflammation in rats. PLoS ONE 2022, 17, e0265430. [Google Scholar] [CrossRef] [PubMed]
- Kato, T.; Yamazaki, K.; Nakajima, M.; Date, Y.; Kikuchi, J.; Hase, K.; Ohno, H.; Yamazaki, K. Oral administration of Porphyromonas gingivalis alters the gut microbiome and serum metabolome. Msphere 2018, 3, e00460-18. [Google Scholar] [CrossRef] [PubMed]
- Zhang, T.; Li, Q.; Cheng, L.; Buch, H.; Zhang, F. Akkermansia muciniphila is a promising probiotic. Microb. Biotechnol. 2019, 12, 1109–1125. [Google Scholar] [CrossRef] [PubMed]
- Abuqwider, J.N.; Mauriello, G.; Altamimi, M. Akkermansia muciniphila, a new generation of beneficial microbiota in modulating obesity: A systematic review. Microorganisms 2021, 9, 1098. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Wang, N.; Tan, H.-Y.; Li, S.; Zhang, C.; Feng, Y. Function of Akkermansia muciniphila in obesity: Interactions with lipid metabolism, immune response and gut systems. Front. Microbiol. 2020, 11, 219. [Google Scholar] [CrossRef]
- Christensen, L.; Sørensen, C.V.; Wøhlk, F.U.; Kjølbæk, L.; Astrup, A.; Sanz, Y.; Hjorth, M.F.; Benítez-Páez, A. Microbial enterotypes beyond genus level: Bacteroides species as a predictive biomarker for weight change upon controlled intervention with arabinoxylan oligosaccharides in overweight subjects. Gut Microbes 2020, 12, 1847627. [Google Scholar] [CrossRef]
- Talavera, K.; Ninomiya, Y.; Winkel, C.; Voets, T.; Nilius, B. Influence of temperature on taste perception. Cell. Mol. Life Sci. 2007, 64, 377–381. [Google Scholar] [CrossRef] [PubMed]
- Stroebele, N.; De Castro, J.M. Effect of ambience on food intake and food choice. Nutrition 2004, 20, 821–838. [Google Scholar] [CrossRef] [PubMed]
- Beker, B.M.; Cervellera, C.; De Vito, A.; Musso, C.G. Human physiology in extreme heat and cold. Int. Arch. Clin. Physiol. 2018, 1, 1–8. [Google Scholar]
Normal | Sweet | Salty | Sour | Bitter | |
---|---|---|---|---|---|
Protein | 178 | 178 | 178 | 178 | 178 |
Carbohydrate | 643 | 628 | 633 | 642 | 643 |
Fat | 70 | 70 | 70 | 70 | 70 |
Amino acid | 1.7 | 1.7 | 1.7 | 1.7 | 1.7 |
Vitamin | 4.8 | 4.8 | 4.8 | 4.8 | 4.8 |
Minerals | 13.7 | 13.7 | 13.7 | 13.7 | 13.7 |
Moisture | 66 | 66 | 66 | 66 | 66 |
Flavor additives | 0 | Sucrose 15 | NaCl 10 | Citric acid 1 | Quinoline 0.008 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, X.; He, H.; Hou, T. Taste Preferences at Different Ambient Temperatures and Associated Changes in Gut Microbiota and Body Weight in Mice. Foods 2024, 13, 2121. https://doi.org/10.3390/foods13132121
Zhang X, He H, Hou T. Taste Preferences at Different Ambient Temperatures and Associated Changes in Gut Microbiota and Body Weight in Mice. Foods. 2024; 13(13):2121. https://doi.org/10.3390/foods13132121
Chicago/Turabian StyleZhang, Xing, Hui He, and Tao Hou. 2024. "Taste Preferences at Different Ambient Temperatures and Associated Changes in Gut Microbiota and Body Weight in Mice" Foods 13, no. 13: 2121. https://doi.org/10.3390/foods13132121
APA StyleZhang, X., He, H., & Hou, T. (2024). Taste Preferences at Different Ambient Temperatures and Associated Changes in Gut Microbiota and Body Weight in Mice. Foods, 13(13), 2121. https://doi.org/10.3390/foods13132121